Cellular mechanisms of arteriogenesis

  • Matthias Heil
  • Wolfgang Schaper
Part of the Experientia Supplementum book series (EXS)


Vascular Endothelial Growth Factor Collateral Vessel Collateral Artery Fluid Shear Stress Smooth Muscle Cell Migration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Maseri A, Araujo L, Finocchiaro M (1993) Collateral development and function in man. In: W Schaper, J Schaper (eds): Collateral circulation: Heart, brain, kidney, limbs. Kluver Academic Publisher, Boston, MA, 381–402Google Scholar
  2. 2.
    Newman MF, Kirchner JL, Phillips-Bute B, Gaver V, Grocott H, Jones RH, Mark DB, Reves JG, Blumenthal JA (2001) Longitudinal assessment of neurocognitive function after coronary-artery bypass surgery. N Engl J Med 344: 395–402PubMedCrossRefGoogle Scholar
  3. 3.
    Mackensen GB, Sato Y, Nellgard B, Pineda J, Newman MF, Warner DS, Grocott HP (2001) Cardiopulmonary bypass induces neurologic and neurocognitive dysfunction in the rat. Anesthesiology 95: 1485–1491PubMedCrossRefGoogle Scholar
  4. 4.
    Fulton W (1963) Arterial anastomoses in the coronary circulation, part 2 (Distribution, enumeration and measurement of arterial anastomoses in health and disease. Scott Med J 8: 466PubMedGoogle Scholar
  5. 5.
    Longland CJ (1953) The collateral circulation of the limb. Ann R Coll Surg Engl 13: 161–164PubMedGoogle Scholar
  6. 6.
    Fulton W (1965) Arterial anastomoses in the coronary circulation. In: W Fulton (ed.): The coronary arteries. Arteriography, microanatomy, and pathogenesis of obliterative coronary artery disease. Thomas, C.C., Springfield, Illinois, 72–128Google Scholar
  7. 7.
    Schaper W, Piek JJ, Munoz-Chapuli R, Wolf C, Ito W (1999) Collateral circulation of the heart. In: JA Ware, M Simons (eds): Angiogenesis and cardiovascular disease. Oxford: Oxford University Press, New York, 159–198Google Scholar
  8. 8.
    Spalteholz W (1924) Die Arterien der Herzwand. Hirzel, Leipzig, 1924Google Scholar
  9. 9.
    Gross L (1921) The blood supply to the heart. Oxford University Press/London and Hoeber, New YorkGoogle Scholar
  10. 10.
    Fulton W (1963) Arterial anastomoses in the coronary circulation. I. Anatomical features in normal and diseased hearts demonstrated by stereoarteriography. Scott Med J 8: 420PubMedGoogle Scholar
  11. 11.
    Scholz D, Ito W, Fleming I, Deindl E, Sauer A, Wiesnet M, Busse R, Schaper J, Schaper W (2000) Ultrastructure and molecular histology of rabbit hind-limb collateral artery growth (arteriogenesis). Virchows Arch 436: 257–270PubMedCrossRefGoogle Scholar
  12. 12.
    Scheel KW, Fitzgerald EM, Martin RO, Larsen RA (1979) The possible role of mechanical stresses on coronary collateral development during gradual coronary occlusion. In: W Schaper (ed.): The pathophysiology of myocardial perfusion. Elsevier/North-Holland, Amsterdam 489–518Google Scholar
  13. 13.
    Cox R (1979) Physiology and hemodynamics of the macrocirculation. In: W Stehbens (ed.): Hemodynamics and the blood vessel wall. Charles C. Thomas, Springfield, IL, 75–156Google Scholar
  14. 14.
    Pipp F, Cai WJ, Boehm S, Karanovic G, Ziegler B, Ritter R, Farzin A, Schmitz-Rixen T, Schaper W (2003) Chronically increased fluid shear stress following arteriovenous-fistula enhances collateral artery growth in a chronic pig hind limb model. FASEB J 17: 338.7Google Scholar
  15. 15.
    Topper JN, Gimbrone MAJr (1999) Blood flow and vascular gene expression: fluid shear stress as a modulator of endothelial phenotype. Mol Med Today 5: 40–546PubMedCrossRefGoogle Scholar
  16. 16.
    Davies PF, Barbee KA, Volin MV, Robotewskyj A, Chen J, Joseph L, Griem ML, Wernick MN, Jacobs E, Polacek DC et al. (1997) Spatial relationships in early signaling events of flow-mediated endothelial mechanotransduction. Annu Rev Physiol 59: 527–549PubMedCrossRefGoogle Scholar
  17. 17.
    Shyy JY, Li YS, Lin MC, Chen W, Yuan S, Usami S, Chien S (1995) Multiple cis-elements mediate shear stress-induced gene expression. J Biomech 28: 1451–1457PubMedCrossRefGoogle Scholar
  18. 18.
    Shyy JY, Lin MC, Han J, Lu Y, Petrime M, Chien S (1995) The cis-acting phorbol ester “12-Otetradecanoylphorbol 13-acetate”-responsive element is involved in shear stress-induced monocyte chemotactic protein 1 gene expression. Proc Natl Acad Sci USA 92: 8069–8073PubMedCrossRefADSGoogle Scholar
  19. 19.
    Resnick N, Collins T, Atkinson W, Bonthron DT, Dewey CF Jr, Gimbrone MA Jr (1993) Plateletderived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element. Proc Natl Acad Sci USA 90: 4591–4595PubMedCrossRefADSGoogle Scholar
  20. 20.
    Ziegelhoeffer T, Scholz D, Friedrich C, Helisch A, Wagner S, Fernandez B, Schaper W (2003) Inhibition of collateral artery growth by mibefradil: Possible role of volume-regulated chloride channels. Endothelium 10: 237–246PubMedCrossRefGoogle Scholar
  21. 21.
    Nishida K, Harrison DG, Navas JP, Fisher AA, Dockery SP, Uematsu M, Nerem RM, Alexander RW, Murphy TJ (1992) Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. J Clin Invest 90: 2092–2096PubMedCrossRefGoogle Scholar
  22. 22.
    Tronc F, Mallat Z, Lehoux S, Wassef M, Esposito B, Tedgui A (2000) Role of matrix metalloproteinases in blood flow-induced arterial enlargement: interaction with NO. Arterioscler Thromb Vasc Biol 20: E120–126PubMedGoogle Scholar
  23. 23.
    Ziche M, Morbidelli L, Choudhuri R, Zhang HT, Donnini S, Granger HJ, Bicknell R (1997) Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest 99: 2625–2634PubMedCrossRefGoogle Scholar
  24. 24.
    RayChaudhury A, Frischer H, Malik AB (1996) Inhibition of endothelial cell proliferation and bFGF-induced phenotypic modulation by nitric oxide. J Cell Biochem 63: 125–134PubMedCrossRefGoogle Scholar
  25. 25.
    Mooradian DL, Hutsell TC, Keefer LK (1995) Nitric oxide (NO) donor molecules: effect of NO release rate on vascular smooth muscle cell proliferation in vitro. J Cardiovasc Pharmacol 25: 674–678PubMedCrossRefGoogle Scholar
  26. 26.
    Tsao PS, Wang B, Buitrago R, Shyy JY, Cooke JP (1997) Nitric oxide regulates monocyte chemotactic protein-1. Circulation 1997;96: 934–940PubMedGoogle Scholar
  27. 27.
    Lloyd PG, Yang HT, Terjung RL (2001) Arteriogenesis and angiogenesis in rat ischemic hindlimb: Role of nitric oxide. Am J Physiol Heart Circ Physiol 281: H2528–2538PubMedGoogle Scholar
  28. 28.
    Matsunaga T, Warltier DC, Weihrauch DW, Moniz M, Tessmer J, Chilian WM (2000) Ischemiainduced coronary collateral growth is dependent on vascular endothelial growth factor and nitric oxide. Circulation 102: 3098–3103PubMedGoogle Scholar
  29. 29.
    Yang HT, Ren J, Laughlin MH, Terjung RL (2002) Prior exercise training produces NO-dependent increases in collateral blood flow after acute arterial occlusion. Am J Physiol Heart Circ Physiol 282: H301–310PubMedGoogle Scholar
  30. 30.
    Wang LH, Chen L (1996) Organization of the gene encoding human prostacyclin synthase. Biochem Biophys Res Commun 226: 631–637PubMedCrossRefGoogle Scholar
  31. 31.
    Heil M, Clauss M, Suzuki K, Buschmann IR, Willuweit A, Fischer S, Schaper W (2000) Vascular endothelial growth factor (VEGF) stimulates monocyte migration through endothelial monolayers via increased integrin expression. Eur J Cell Biol 79: 850–857PubMedCrossRefGoogle Scholar
  32. 32.
    Takagi J, Springer TA (2002) Integrin activation and structural rearrangement. Immunol Rev 186: 141–163PubMedCrossRefGoogle Scholar
  33. 33.
    Hogg N, Henderson R, Leitinger B, McDowall A, Porter J, Stanley P (2002) Mechanisms contributing to the activity of integrins on leukocytes. Immunol Rev 186: 164–171PubMedCrossRefGoogle Scholar
  34. 34.
    Scholz D, Ziegelhoeffer T, Helisch A, Wagner S, Friedrich C, Podzuweit T, Schaper W (2002) Contribution of arteriogenesis and angiogenesis to postocclusive hindlimb perfusion in mice. J Mol Cell Cardiol 34: 775–787PubMedCrossRefGoogle Scholar
  35. 35.
    Carlos TM, Harlan JM (1994) Leukocyte-endothelial adhesion molecules. Blood 84: 2068–2101PubMedGoogle Scholar
  36. 36.
    Schaper J, Konig R, Franz D, Schaper W (1976) The endothelial surface of growing coronary collateral arteries. Intimal margination and diapedesis of monocytes. A combined SEM and TEM study. Virchows Arch A Pathol Anat Histol 370: 193–205PubMedCrossRefGoogle Scholar
  37. 37.
    Heil M, Ziegelhoeffer T, Pipp F, Kostin S, Martin S, Clauss M, Schaper W (2002) Blood monocyte concentration is critical for enhancement of collateral artery growth. Am J Physiol Heart Circ Physiol 283: H2411–2419PubMedGoogle Scholar
  38. 38.
    Pipp F, Heil M, Issbrucker K, Ziegelhoeffer T, Martin S, van den Heuvel J, Weich H, Fernandez B, Golomb G, Carmeliet P et al. (2003) VEGFR-1-selective VEGF homologue PlGF is arteriogenic: Evidence for a monocyte-mediated mechanism. Circ Res 2003;92: 378–385PubMedCrossRefGoogle Scholar
  39. 39.
    Ito WD, Arras M, Winkler B, Scholz D, Schaper J, Schaper W (1997) Monocyte chemotactic protein-1 increases collateral and peripheral conductance after femoral artery occlusion. Circ Res 80: 829–837PubMedGoogle Scholar
  40. 40.
    Hoefer IE, van Royen N, Buschmann IR, Piek JJ, Schaper W (2001) Time course of arteriogenesis following femoral artery occlusion in the rabbit. Cardiovasc Res 49: 609–617PubMedCrossRefGoogle Scholar
  41. 41.
    Voskuil M (2003) Abnormal monocyte recruitment and collateral artery formation in monocyte chemoattractant protein-1 deficient mice. In: Experimental and clinical studies on collateral and epicardial flow in obstructive arterial disease (Thesis). Universiteit van Amsterdam, Amsterdam, 25–35Google Scholar
  42. 42.
    Kuziel WA, Morgan SJ, Dawson TC, Griffin S, Smithies O, Ley K, Maeda N (1997) Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc Natl Acad Sci USA 94: 12053–12058PubMedCrossRefADSGoogle Scholar
  43. 43.
    Heil M, Ziegelhoeffer T, Wagner S, Fernandez B, Helisch A, Martin S, Tribulova S, Kuziel WA, Bachmann G, Schaper W (2004) Collateral artery growth (arteriogenesis) after experimental arterial occlusion is impaired in mice lacking CC-chemokine receptor-2. Circ Res 94: 671–677PubMedCrossRefGoogle Scholar
  44. 44.
    Risau W (1997) Mechanisms of angiogenesis. Nature 386: 671–674PubMedCrossRefGoogle Scholar
  45. 45.
    Clauss M, Weich H, Breier G, Knies U, Rockl W, Waltenberger J, Risau W (1996) The vascular endothelial growth factor receptor Flt-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J Biol Chem 271: 17629–17634PubMedCrossRefGoogle Scholar
  46. 46.
    Wiseman DM, Polverini PJ, Kamp DW, Leibovich SJ (1988) Transforming growth factor-beta (TGF beta) is chemotactic for human monocytes and induces their expression of angiogenic activity. Biochem Biophys Res Commun 157: 793–800PubMedCrossRefGoogle Scholar
  47. 47.
    Chantry D, Turner M, Abney E, Feldmann M (1989) Modulation of cytokine production by transforming growth factor-beta. J Immunol 142: 4295–4300PubMedGoogle Scholar
  48. 48.
    Scholz D, Cai WJ, Schaper W (2001) Arteriogenesis, a new concept of vascular adaptation in occlusive disease. Angiogenesis 4: 247–257PubMedCrossRefGoogle Scholar
  49. 49.
    Ziegelhoeffer T, Hoefer I, van Royen N, Buschmann I (1999) Effective reduction in collateral artery formation through matrix metalloproteinase inhibitors. Circulation 100: I–705Google Scholar
  50. 50.
    Deindl E, Ziegelhoffer T, Kanse SM, Fernandez B, Neubauer E, Carmeliet P, Preissner KT, Schaper W (2003) Receptor-independent role of the urokinase-type plasminogen activator during arteriogenesis. FASEB J 17: 1174–1176PubMedGoogle Scholar
  51. 51.
    Sitrin RG, Shollenberger SB, Strieter RM, Gyetko MR (1996) Endogenously produced urokinase amplifies tumor necrosis factor-alpha secretion by THP-1 mononuclear phagocytes. J Leukocyte Biol 59: 302–311PubMedGoogle Scholar
  52. 52.
    Carmeliet P, Moons L, Dewerchin M, Rosenberg S, Herbert JM, Lupu F, Collen D (1998) Receptor-independent role of urokinase-type plasminogen activator in pericellular plasmin and matrix metalloproteinase proteolysis during vascular wound healing in mice. J Cell Biol 140: 233–245PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag/Switzerland 2005

Authors and Affiliations

  • Matthias Heil
    • 1
  • Wolfgang Schaper
    • 1
  1. 1.Department of Experimental CardiologyMax-Planck-Institute for Physiological and Clinical ResearchBad NauheimGermany

Personalised recommendations